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The Mitochondrial Genomes of the Acoelomorph Worms Paratomella Rubra and Isodiametra Pulchra

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The Mitochondrial Genomes of the Acoelomorph Worms Paratomella Rubra and Isodiametra Pulchra bioRxiv preprint doi: https://doi.org/10.1101/103556; this version posted January 26, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. The mitochondrial genomes of the acoelomorph worms Paratomella rubra and Isodiametra pulchra Helen E Robertson1, François Lapraz1,2, Bernhard Egger1,3, Maximilian J Telford1 and Philipp H. Schiffer1 1Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT 2CNRS/UMR 7277, institut de Biologie Valrose, iBV, Université de Nice Sophia Antipolis, Parc Valrose, Nice cedex 2, France (current address) oute de Narbonne, Toulouse, France (current address) 3Institute of Zoology, University of Innsbruck, Technikerstr. 25, 6020 Innsbruck, Austria (current address) *Authors for communication: [email protected], [email protected] ORCiDs HER: 0000-0001-7951-0473 FL: 0000-0001-9209-2018 MJT: 0000-0002-3749-5620 PHS: 0000-0001-6776-0934 Abstract Acoels are small, ubiquitous, but understudied, marine worms with a very simple body plan. Their internal phylogeny is still in parts unresolved, and the position of their proposed phylum Xenacoelomorpha (Xenoturbella+Acoela) is still debated. Here we describe mitochondrial genome sequences from two acoel species: Paratomella rubra and Isodiametra pulchra. The 14,954 nucleotide-long P. rubra sequence is typical for metazoans in size and gene content. The larger I. pulchra mitochondrial genome contains both ribosomal genes, 21 tRNAs, but only 11 protein-coding genes. We find evidence suggesting a duplicated sequence in the I. pulchra mitochondrial genome. Mitochondrial sequences for both P. rubra and I. pulchra have a unique genome organisation in comparison to other published metazoan mitochondrial genomes. We found a large degree of protein-coding gene and tRNA overlap in P. rubra, with little non-coding sequence making the genome compact. Conversely, the I. pulchra mitochondrial genome has many long non-coding sequences between genes, likely driving the genome size expansion. Phylogenetic trees inferred from concatenated alignments of mitochondrial genes grouped the fast-evolving Acoela and Tunicata, almost certainly due to the systematic error of long branch attraction: a reconstruction artefact that is probably compounded by the fast substitution rate of mitochondrial genes in this taxon. 1 bioRxiv preprint doi: https://doi.org/10.1101/103556; this version posted January 26, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Introduction Acoel flatworms are small, soft-bodied, unsegmented, marine animals lacking a gut epithelium, coelomic cavity, and anus. Instead, they typically possess a ventral mouth opening, and a simple syncytial digestive system1. Due primarily to the common attributes of acoelomate body and the absence of a through gut, Acoela were traditionally grouped as an order within the Platyhelminthes. The first molecular systematic studies on these animals using small subunit (SSU) ribosomal RNA gene sequences revealed that the Acoelomorpha are in fact a distinct lineage, quite separate from the main clade of the Platyhelminthes (Rhabditophora and Catenulida)2-4. Instead, these initial molecular studies supported a position of the Acoelomorpha diverging prior to the protostome/deuterostome common ancestor. More recently, the Acoelomorpha have been linked to the similarly simple marine worm Xenoturbella in the new phylum Xenacoelomorpha, making sense of their shared simple body plan and other shared morphological characters, such as unusual ciliary ultrastructure5 and their simple basiepidermal nervous system6. Despite considerable efforts, the position of Xenacoelomorpha within the Metazoa remains unresolved, with alternative lines of evidence placing them either as the sister group to the remaining Bilateria (protostomes and deuterostomes)7,8, or as a phylum within the deuterostomes9. A better understanding of acoel phylogeny and evolution is therefore integral to answering central questions concerning the evolution of Bilateria and its subtaxa. To this end more genomic data are needed. Metazoan mitochondrial DNA (mtDNA) is a closed-circular molecule typically comprising 37 genes which are, for the most part, invariant across the Metazoa10. These include the two rRNAs of the mitochondrial ribosome, 22 tRNAs necessary for translation, and 13 protein-coding genes for the enzymes of oxidative phosphorylation. atp8 is the only gene known to have been commonly lost from this complement, and this has been observed in a number of independent metazoan lineages, including the acoel Symsagittifera roscoffensis11. In addition to primary sequence data, mtDNA has a number of other features which can be used for phylogenetic inference, including variations in mitochondrial genetic code12; a higher rate of sequence evolution than nuclear DNA13; changes in gene order and changes in the secondary structure of rRNAs and tRNAs14. Mitochondrial gene sequences have been used extensively for phylogenetic inference. In a recent paper, Rouse et al. used mitochondrial protein-coding sequence data from four newly discovered species of Xenoturbella (X. hollandorum, X. churro, X. monstrosa and X. profunda) to infer the internal phylogeny of the Xenoturbellida15. Wider phylogenetic inference including mitochondrial proteins from these species placed Xenacoelomorpha with the deuterostomes15, corroborating previous mitochondrial phylogenetic analysis of this phylum9,16,17. 2 bioRxiv preprint doi: https://doi.org/10.1101/103556; this version posted January 26, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Mitochondrial gene content is largely invariable across the Metazoa, with the order in which genes are arranged being fairly stable and conserved for up to hundreds of millions of years in some metazoan lineages. Rearrangement events, thought to occur via a model of ‘duplication and deletion’14,18, whereby a portion of the mitochondrial genome is duplicated, and the original copy of the duplicated gene subsequently deleted, are rare. The infrequency of such rearrangements, and the huge number of possible rearrangement scenarios, means that convergence on the same gene order in unrelated lineages is unlikely. Gene order is thus likely to retain evolutionary signals, with a common gene order being indicative of common ancestry and informative for the study of metazoan divergence19. Rearrangement of genes within the mitochondrial genome of different species can be a particularly powerful tool in the analysis of phylogenetic relationships14 and may also indicate accelerated evolution in a taxon. In this study, we describe the mitochondrial genomes from two species of acoel: Paratomella rubra and Isodiametra pulchra. Adult specimens of both animals are approximately 1mm in length, and, as is typical for small acoel species, they occupy the littoral and sub-littoral zones of marine ecosystems: P. rubra has been described across Europe and North America20,21, and I. pulchra lives abundantly in the mud flats of Maine22. Both species move freely within the sediment by gliding on a multiciliated epidermis. First described by Rieger and Ott21, P. rubra is an elongate and flattened worm belonging to the family Paratomellidae, which is sister group to all other described acoel species23,24. A 9.7kb fragment of mitochondrial genome has previously been described from specimens of P. rubra collected on the Mediterranean coast of Spain25. I pulchra belongs to the family Isodiametridae; it can be maintained long-term in culture and has been used experimentally for in situ hybridisation, RNAi, and other molecular protocols 22,26,27. It's use as a ‘model acoel’ therefore makes this species particularly valuable for investigation. Results Genomic Composition We assembled 14,954 base pairs of the P. rubra mitochondrial genome, starting from three genome assembly fragments and using Sanger sequencing of PCR fragments (Fig. 1a). We were unable to close the circular mitochondrial genome of P. rubra, but our 14.9kb sequence contains all 13 protein-coding genes, both ribosomal genes and 22 putative tRNAs. Compared to the fragment of the genome previously published we have found four additional protein-coding genes and 12 additional tRNAs 25. All genes are found exclusively on one strand of the sequence. Allowing for overlap, protein-coding genes account for 74.79% of the genomic sequence; ribosomal genes 13.95%; tRNA genes 9.10% and non-coding DNA 2.04%. A 156 nucleotide-long stretch of non-coding sequence is found between cytochrome c oxidase subunit 2 (cox2) and NADH dehydrogenase subunit 1 (nad1). 3 bioRxiv preprint doi: https://doi.org/10.1101/103556; this version posted January 26, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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